Focal switching of photochromic fluorescent proteins enables multiphoton microscopy with superior image contrast

Biomedical Optics Express

Volumn 3, Issue 8, 2012, Pages 1955-1963

  Kao, Ya Ting ^a   Zhu, Xinxin ^a   Xu, Fang ^a   Min, Wei ^a  

^a Department of Chemistry Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENCE; FLUORESCENCE MICROSCOPY; SCATTERING; TISSUE;

BIOLOGICAL STRUCTURES; DARK STATE; FLUORESCENT PROTEIN; FOCAL SWITCH; IMAGE CONTRASTS; IMAGING DEPTH; IMAGING PROBE; IMAGING-DEPTH LIMIT; INCIDENT LASER; LIGHT ILLUMINATION; MULTI-PHOTON MICROSCOPY; MULTIPHOTON FLUORESCENCE MICROSCOPY; MULTIPHOTONS; NONLINEAR EXCITATION; OPTICAL IMAGING MODALITIES; OUT-OF-FOCUS; SCATTERING LOSS; SWITCHABLE; TISSUE PHANTOM;

PROTEINS;

EID: 84865638260     PISSN: None     EISSN: 21567085     Source Type: Journal    
DOI: 10.1364/BOE.3.001955     Document Type: Article

References (37)

1. W. Denk, J. H. Strickler, and W. W. Webb, "Two-photon laser scanning fluorescence microscopy, " Science 248(4951), 73-76 (1990).
2. W. R. Zipfel, R. M. Williams, and W. W. Webb, "Nonlinear magic: multiphoton microscopy in the biosciences, " Nat. Biotechnol. 21(11), 1369-1377 (2003).
3. F. Helmchen and W. Denk, "Deep tissue two-photon microscopy, " Nat. Methods 2(12), 932-940 (2005).
4. J. N. D. Kerr and W. Denk, "Imaging in vivo: watching the brain in action, " Nat. Rev. Neurosci. 9(3), 195-205 (2008).
5. B. R. Masters and P. T. C. So, Handbook of Biomedical Nonlinear Optical Microscopy (Oxford University Press, 2008).
6. R. Yuste, ed., Imaging: A Laboratory Manual (Cold Spring Harbor Press, 2010).
7. J. Ying, F. Liu, and R. R. Alfano, "Spatial distribution of two-photon-excited fluorescence in scattering media, " Appl. Opt. 38(1), 224-229 (1999).
8. P. Theer, M. T. Hasan, and W. Denk, "Two-photon imaging to a depth of 1000 μm in living brains by use of a Ti:Al2O3 regenerative amplifier, " Opt. Lett. 28(12), 1022-1024 (2003).
9. P. Theer and W. Denk, "On the fundamental imaging-depth limit in two-photon microscopy, " J. Opt. Soc. Am. A 23(12), 3139-3149 (2006).
10. D. Kobat, N. G. Horton, and C. Xu, "In vivo two-photon microscopy to 1.6-mm depth in mouse cortex, " J. Biomed. Opt. 16(10), 106014 (2011).
11. N. J. Durr, C. T. Weisspfennig, B. A. Holfeld, and A. Ben-Yakar, "Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues, " J. Biomed. Opt. 16(2), 026008 (2011).
12. M. Rueckel, J. A. Mack-Bucher, and W. Denk, "Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing, " Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137-17142 (2006).
13. N. Ji, D. E. Milkie, and E. Betzig, "Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues, " Nat. Methods 7(2), 141-147 (2010).
14. D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, "Deep tissue multiphoton microscopy using longer wavelength excitation, " Opt. Express 17(16), 13354-13364 (2009).
15. Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, "Optical phase conjugation for turbidity suppression in biological samples, " Nat. Photonics 2(2), 110-115 (2008).
16. H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, "Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain, " Nat. Neurosci. 14(11), 1481-1488 (2011).
17. A. Leray, K. Lillis, and J. Mertz, "Enhanced background rejection in thick tissue with differential-aberration twophoton microscopy, " Biophys. J. 94(4), 1449-1458 (2008).
18. N. Chen, C.-H. Wong, and C. J. Sheppard, "Focal modulation microscopy, " Opt. Express 16(23), 18764-18769 (2008).
19. J. Lippincott-Schwartz and G. H. Patterson, "Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging, " Trends Cell Biol. 19(11), 555-565 (2009).
20. D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, "Fluorescent proteins and their applications in imaging living cells and tissues, " Physiol. Rev. 90(3), 1103-1163 (2010).
21. B. Wu, K. D. Piatkevich, T. Lionnet, R. H. Singer, and V. V. Verkhusha, "Modern fluorescent proteins and imaging technologies to study gene expression, nuclear localization, and dynamics, " Curr. Opin. Cell Biol. 23(3), 310-317 (2011).
22. R. Ando, H. Mizuno, and A. Miyawaki, "Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting, " Science 306(5700), 1370-1373 (2004).
23. M. Hofmann, C. Eggeling, S. Jakobs, and S. W. Hell, "Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins, " Proc. Natl. Acad. Sci. U.S.A. 102(49), 17565-17569 (2005).
24. C. Flors, J. Hotta, H. Uji-i, P. Dedecker, R. Ando, H. Mizuno, A. Miyawaki, and J. Hofkens, "A stroboscopic approach for fast photoactivation-localization microscopy with Dronpa mutants, " J. Am. Chem. Soc. 129(45), 13970-13977 (2007).
25. M. Andresen, A. C. Stiel, J. Fölling, D. Wenzel, A. Schönle, A. Egner, C. Eggeling, S. W. Hell, and S. Jakobs, "Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy, " Nat. Biotechnol. 26(9), 1035-1040 (2008).
26. E. H. Rego, L. Shao, J. J. Macklin, L. Winoto, G. A. Johansson, N. Kamps-Hughes, M. W. Davidson, and M. G. L. Gustafsson, "Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution, " Proc. Natl. Acad. Sci. U.S.A. 109(3), E135-E143 (2012).
27. M. Heilemann, P. Dedecker, J. Hofkens, and M. Sauer, "Photoswitches: key molecules for subdiffractionresolution fluorescence imaging and molecular quantification, " Laser Photon. Rev. 3(1-2), 180-202 (2009).
28. K. Isobe, A. Suda, H. Hashimoto, F. Kannari, H. Kawano, H. Mizuno, A. Miyawaki, and K. Midorikawa, "Highresolution fluorescence microscopy based on a cyclic sequential multiphoton process, " Biomed. Opt. Express 1(3), 791-797 (2010).
29. G. Marriott, S. Mao, T. Sakata, J. Ran, D. K. Jackson, C. Petchprayoon, T. J. Gomez, E. Warp, O. Tulyathan, H. L. Aaron, E. Y. Isacoff, and Y. Yan, "Optical lock-in detection imaging microscopy for contrast-enhanced imaging in living cells, " Proc. Natl. Acad. Sci. U.S.A. 105(46), 17789-17794 (2008).
30. S. Mao, R. K. P. Benninger, Y. Yan, C. Petchprayoon, D. Jackson, C. J. Easley, D. W. Piston, and G. Marriott, "Optical lock-in detection of FRET using synthetic and genetically encoded optical switches, " Biophys. J. 94(11), 4515-4524 (2008).
31. F. V. Subach, L. Zhang, T. W. J. Gadella, N. G. Gurskaya, K. A. Lukyanov, and V. V. Verkhusha, "Red fluorescent protein with reversibly photoswitchable absorbance for photochromic FRET, " Chem. Biol. 17(7), 745-755 (2010).
32. Y.-T. Kao, X. Zhu, and W. Min, "Protein-flexibility mediated coupling between photoswitching kinetics and surrounding viscosity of a photochromic fluorescent protein, " Proc. Natl. Acad. Sci. U.S.A. 109(9), 3220-3225 (2012).
33. R. Ando, C. Flors, H. Mizuno, J. Hofkens, and A. Miyawaki, "Highlighted generation of fluorescence signals using simultaneous two-color irradiation on Dronpa mutants, " Biophys. J. 92(12), L97-L99 (2007).
34. M. Andresen, A. C. Stiel, S. Trowitzsch, G. Weber, C. Eggeling, M. C. Wahl, S. W. Hell, and S. Jakobs, "Structural basis for reversible photoswitching in Dronpa, " Proc. Natl. Acad. Sci. U.S.A. 104(32), 13005-13009 (2007).
35. M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, "Two-photon absorption properties of fluorescent proteins, " Nat. Methods 8(5), 393-399 (2011).
36. T. Grotjohann, I. Testa, M. Leutenegger, H. Bock, N. T. Urban, F. Lavoie-Cardinal, K. I. Willig, C. Eggeling, S. Jakobs, and S. W. Hell, "Diffraction-unlimited all-optical imaging and writing with a photochromic GFP, " Nature 478(7368), 204-208 (2011).
37. L. Wei, Z. Chen, and W. Min, "Stimulated emission reduced fluorescence microscopy: a concept for extending the fundamental depth limit of two-photon fluorescence imaging, " Biomed. Opt. Express 3(6), 1465-1475 (2012).